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The phrase His Majesty's Opposition was coined in 1826, before the advent of the modern two-party system, when Parliament consisted more of interests, relationships and factions rather than the highly coherent political parties of today (although the Whigs and Tories were the two main parties). The phrase was originally coined in jest; in attacking Foreign Secretary, George Canning, in the House of Commons, John Hobhouse said jokingly, "It is said to be hard on His Majesty's Ministers to raise objections of this character but it is more hard on His Majesty's Opposition to compel them to take this course."

Whilst most days in the House of Commons are set aside for government business, twenty days in each session are set aside for opposition debates. Of these days, seventeen are at the disposal of the Leader of the Opposition and three can be used by the leader of the smaller, or Tertiary, opposition party (for most recent history this has been the Liberal Democrats, though currently they have been replaced by the Scottish National Party).[1]

Although the Opposition has no more formal powers in setting the Parliamentary agenda, in reality they have a certain influence through a process known as the usual channels.[1]

The Leader of Her Majesty's Most Loyal Opposition is often seen as the Prime Minister-in-waiting; as well as his salary as an MP, he or she receives a statutory salary and perquisites like those of a cabinet minister, including appointment as a Privy Councillor. Since 1915, the Leader of the Opposition has, like the Prime Minister, always been a member of the House of Commons. Before that a member of the House of Lords sometimes took on the role, although often there was no overall Leader of the Opposition.

Although there has never been a dispute as to who holds the position, under the Ministerial and other Salaries Act 1975, the Speaker’s decision on the identity of the Leader of the Opposition is final.[1]

The most public parliamentary function of the Leader of the Opposition is Prime Minister's Questions (PMQs), currently a 30-minute session held on Wednesday at 12 PM when Parliament is sitting. The Leader of the Opposition has six questions, which s/he sometimes splits into two sets. Other backbench opposition MPs also have the right to question the Prime Minister; they are selected either through a ballot, or by "catching the Speaker's eye". By convention, other Shadow Cabinet members do not question the Prime Minister at PMQs, except when standing-in for the Leader.

Every government department is subjected to questions in the House of Commons and the House of Lords. As with PMQs, the official opposition spokesmen are allocated a number of questions, and in addition backbench MPs are free to ask questions. In the House of Lords, opposition spokespeople also question the government. This is one of the reasons why every government department (and opposition shadow department) has at least one member of parliament and one peer in it.

As is usual with Westminster systems, and other statutory assemblies and councils in the UK, the government and its supporters sit to the Speaker's right, whilst the Opposition parties sit to his/her left.[2] Currently, members from the Conservative party sit to the Speaker's right, and members from the Labour Party sit on the main left bench, which is where the main opposition party sit. The second main opposition bench is where the third largest party sits, in this case the SNP. The back of this bench is where other minor parties sit, such as the Liberal Democrats, Democratic Unionist Party, Plaid Cymru, UKIP and The Green Party.